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The identification of candidate rice genes that confer resistance to the brown planthopper (Nilaparvata lugens) through representational difference analysis

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Abstract

The development of rice varieties (Oryza sativa L.) that are resistant to the brown planthopper (BPH; Nilaparvata lugens Stål) is an important objective in current breeding programs. In this study, we generated 132 BC5F5 near-isogenic rice lines (NILs) by five backcrosses of Samgangbyeo, a BPH resistant indica variety carrying the Bph1 locus, with Nagdongbyeo, a BPH susceptible japonica variety. To identify genes that confer BPH resistance, we employed representational difference analysis (RDA) to detect transcripts that were exclusively expressed in one of our BPH resistant NIL, SNBC61, during insect feeding. The chromosomal mapping of the RDA clones that we subsequently isolated revealed that they are located in close proximity either to known quantitative trait loci or to an introgressed SSR marker from the BPH resistant donor parent Samgangbyeo. Genomic DNA gel-blot analysis further revealed that loci of all RDA clones in SNBC61 correspond to the alleles of Samgangbyeo. Most of the RDA clones were found to be exclusively expressed in SNBC61 and could be assigned to functional groups involved in plant defense. These RDA clones therefore represent candidate defense genes for BPH resistance.

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References

  • Alam SN, Cohen MB (1998) Detection and analysis of QTLs for resistance to the brown planthopper, Nilaparvata lugens, in a doubled-haploid rice population. Theor Appl Genet 97:1370–1379

    Article  CAS  Google Scholar 

  • Baldwin IT, Preston CA (1999) The eco-physiological complexity of plant responses to insect herbivores. Planta 208:137–145

    Article  CAS  Google Scholar 

  • Becerra C, Jahrmann T, Puigdomènech P, Vicient CM (2004) Ankyrin repeat-containing proteins in Arabidopsis: characterization of a novel and abundant group of genes coding ankyrin-transmembrane proteins. Gene 340:111–121

    Article  PubMed  CAS  Google Scholar 

  • Bosque-Pérez NA, Buddenhagen IW (1992) The development of host–plant resistance to insect pests: outlook for the tropics. In: Menken SBJ, Visser JH, Harrewijn P (eds) Proceedings 8th international symposium insect–plant relationships. Kluwer, Dordrecht, pp 235–249

    Google Scholar 

  • Briggs DE (1992) Barley germination: biochemical changes and hormonal control. In: Shewry PR (ed) Barley: genetics, biochemistry, molecular biology and biotechnology. C.A.B. International, Wallingford, pp 369–401

    Google Scholar 

  • Brotman Y, Silberstein L, Kovalski I, Perin C, Dogimont C, Pitrat M, Klingler J, Thompson GA, Perl-Treves R (2002) Resistance gene homologues in melon are linked to genetic loci conferring disease and pest resistance. Theor Appl Genet 104:1055–1063

    Article  PubMed  CAS  Google Scholar 

  • Cao H, Glazebrook J, Clarke JD, Volko S, Dong X (1997) The Arabidopsis npr1 gene that controls systemic acquired resistance encodes a novel protein containing ankyrin repeats. Cell 88:57–63

    Article  PubMed  CAS  Google Scholar 

  • Chen JW, Wang L, Pang XF, Pan QH (2006) Genetic analysis and fine mapping of a rice brown planthopper (Nilaparvata lugens Stål) resistance gene bpb19(t). Theor Appl Genet 275:321–329

    CAS  Google Scholar 

  • Cho JI, Ryoo N, Ko S, Lee SK, Lee J, Jung KH, Lee YH, Bhoo SH, Winderickx J, An G, Hahn TR, Jeon JS (2006) Structure, expression, and functional analysis of the hexokinase gene family in rice (Oryza sativa L.). Planta 224:598–611

    Article  PubMed  CAS  Google Scholar 

  • Cohen MB, Alam SN, Medina EB, Bernal CC (1997) Brown planthopper, Nilaparvata lugens, resistance in rice cultivar IR64, In: mechanism and role in successful N. lugens management in Central Luzon, Philippines. Entomol Exp Appl 85:221–229

    Article  Google Scholar 

  • Devoto A, Muskett PR, Shirasu K (2003) Role of ubiquitination in the regulation of plant defence against pathogens. Curr Opin Plant Biol 6:307–311

    Article  PubMed  CAS  Google Scholar 

  • Diatchenko L, LauYFC, Campbell AP, Chenchik A, Moqadam F, Huang B, Lukyanov S, Lukyanov K, Gurskaya N, Sverdlov E, Siebert PD (1996) Suppression subtractive hybridization: a method for generating differentially regulated or tissue-specific cDNA probes and libraries. Proc Natl Acad Sci USA 93:6025–6030

    Article  PubMed  CAS  Google Scholar 

  • Hayashi H, Chino M (1990) Chemical composition of phloem sap from the uppermost internode of the rice plant. Plant Cell Physiol 31:247–251

    CAS  Google Scholar 

  • Heinrichs EA (1979) Control of leafhopper and planthopper vectors of rice viruses. In: Moramorosch K, Harris KF (eds) Leafhopper vectors and plant disease agents. Academic Press, New York, pp 529–558

    Google Scholar 

  • Heinrichs EA (1986) Perspectives and directions for the continued development of insect-resistant rice varieties. Agric Ecosyst Environ 18:9–36

    Article  Google Scholar 

  • Hermsmeier D, Schittko U, Baldwin IT (2001) Molecular interactions between the specialist herbivore Manduca sexta (Lepidoptera, Sphingidae) and its natural host Nicotiana attenuata. I. Large-scale changes in the accumulation of growth- and defense-related plant mRNAs. Plant Physiol 125:683–700

    Article  PubMed  CAS  Google Scholar 

  • Hirabayashi H, Angeles ER, Kaji R, Ogawa T, Brar DS, Khush GS (1998) Identification of brown planthopper resistance gene derived from O. officinalis using molecular markers in rice (in Japanese). Breed Sci Suppl 48:82

    Google Scholar 

  • Hoson T (1993) Regulation of polysaccharide breakdown during auxin-induced cell wall loosening. J Plant Res 106:369–381

    Article  CAS  Google Scholar 

  • Howe GA, Lightner J, Browse J, Ryan CA (1996) An octadecanoid pathway mutant (JL5) of tomato is compromised in signaling for defense against insect attack. Plant Cell 8:2067–2077

    Article  PubMed  CAS  Google Scholar 

  • Huang N, Parco A, Mew T, Magpantay G, McCouch S, Guiderdoni E, Xu J, Subudhi P, Angeles ER, Khush GS (1997) RFLP mapping of isozymes, RAPD and QTLs for grain shape, brown planthopper resistance in a double-haploid population. Mol Breed 3:105–113

    Article  CAS  Google Scholar 

  • Huang Z, He G, Shu L, Li X, Zhang Q (2001) Identification and mapping of two brown planthopper resistance genes in rice. Theor Appl Genet 102:929–934

    Article  CAS  Google Scholar 

  • Hubank M, Schatz DG (1994) Identifying differences in mRNA expression by representational difference analysis of cDNA. Nucleic Acids Res 22:5640–5648

    Article  PubMed  CAS  Google Scholar 

  • Hui D, Iqbal J, Lehmann K, Gase K, Saluz HP, Baldwin IT (2003) Molecular interaction between the specialist herbivore Manduca sexta (Lepidoptera, Sphingidae) and its natural host Nicotiana attenuata: V. Microarray analysis and further characterization of large-scale changes in herbivore-induced mRNAs. Plant Physiol 131:1877–1893

    Article  PubMed  CAS  Google Scholar 

  • Inouhe M, McCellan M, Nevins D (1997) Developmental regulation of polysaccharide metabolism and growth in primary cell walls of maize. Int J Biol Macromol 21:21–28

    Article  PubMed  CAS  Google Scholar 

  • International Rice Genome Sequencing Project (2005) The map-based sequence of the rice genome. Nature 436:793–800

    Article  CAS  Google Scholar 

  • Ishii T, Brar DS, Multani DS, Khush GS (1994) Molecular tagging of genes for brown planthopper resistance and earliness introgressed from Oryza australiensis into cultivated rice, O. sativa. Genome 37:217–221

    Article  CAS  PubMed  Google Scholar 

  • Jantasuriyarat C, Gowda M, Haller K, Hatfield J, Lu G, Stahlberg E, Zhou B, Li H, Kim HR, Yu Y, Dean RA, Wing RA, Soderlund C, Wang GL, Wing R (2005) Large-scale identification of expressed sequence tags involved in rice and rice blast fungus interaction. Plant Physiol 138:105–115

    Article  PubMed  Google Scholar 

  • Jena KK, Jeung JU, Lee JH, Choi HC, Brar DS (2006) High-resolution mapping of a new brown planthopper (BPH) resistance gene, Bph18(t), and marker-assisted selection for BPH resistance in rice (Oryza sativa L.). Theor Appl Genet 112:288–297

    Article  PubMed  CAS  Google Scholar 

  • Jeon J-S, Lee S, Jung K-H, Jun S-H, Kim C, An G (2000) Tissue-preferential expression of a rice α-Tubulin gene, OsTubA1, mediated by the first intron. Plant Physiol 123:1005–1014

    Article  PubMed  CAS  Google Scholar 

  • Kaloshian I (2004) Gene-for-gene disease resistance: bridging insect pest and pathogen defence. J Chem Ecol 30:2419–2438

    Article  PubMed  CAS  Google Scholar 

  • Kaloshian I, Lange WH, Willamson VM (1995) An aphid resistance locus is tightly linked to the nematode resistance gene, Mi, in tomato. Proc Natl Acad Sci USA 92:622–625

    Article  PubMed  CAS  Google Scholar 

  • Keyan ZS, Bi JL, Liui TX (2005) Molecular strategies of plant defense and insect counter-defense. Insect Sci 12:3–15

    Article  Google Scholar 

  • Khush GS (1979) Genetics of and breeding for resistance to brown planthopper. Threat to rice production in Asia. International Rice Research Institute, Los Banos, pp 321–332

    Google Scholar 

  • Khush GS (1989) Multiple disease and insect resistance for increased yield stability in rice. In: IRRI (ed) Progress in irrigated rice research. International Rice Research Institute, Manila, pp 79–92

  • Lee JH, Yeo US, Kwak DY, Park DS, Oh BG, Ku YC, Kim HY, Sohn JK (2005) QTL analysis for ripening traits of BPH resistant backcross inbreed lines in rice. Korean J Breed 37:295–299

    Google Scholar 

  • Liu GQ, Yan HH, Fu Q, Qian Q, Zhang ZT, Zhai WX, Zhu LH (2001) Mapping of a new gene for brown planthopper resistance in cultivated rice introgressed from Oryza eichingeri. Chin Sci Bull 46:1459–1462

    CAS  Google Scholar 

  • McElroy D, Zhang W, Cao J, Wu R (1990) Isolation of an efficient actin promotor for use in rice transformation. Plant Cell 2:163–171

    Article  PubMed  CAS  Google Scholar 

  • Michael JO, Andrew HS (1997) Isolation of rare transcripts by representational difference analysis. Nucleic Acids Res 25:2681–2682

    Article  Google Scholar 

  • Moran PJ, Thompson GA (2001) Molecular responses to aphid feeding in Arabidopsis in relation to plant defense pathways. Plant Physiol 125:1074–1085

    Article  PubMed  CAS  Google Scholar 

  • Moran PJ, Cheng Y, Cassell JL, Thompson GA (2002) Gene expression profiling of Arabidopsis thaliana in compatible plant–aphid interactions. Arch Insect Biochem Physiol 51:182–203

    Article  PubMed  CAS  Google Scholar 

  • Panaud O, Vitte C, Hivert J, Muzlak S, Talag J, Brar D, Sarr A (2002) Characterization of transposable elements in the genome of rice (Oryza sativa L.) using Representational Difference Analysis (RDA). Mol Genet Genomics 268:113–121

    Article  PubMed  CAS  Google Scholar 

  • Park SJ, Huang Y, Ayoubi P (2005) Identification of expression profiles of sorghum genes in response to greenbug phloem feeding using cDNA subtraction and microarray analysis. Planta 223:932–947

    Article  PubMed  CAS  Google Scholar 

  • Pastorian K, Hawel III L, Byus CV (2000) Optimization of cDNA representational difference analysis for the identification of differentially expressed mRNAs. Anal Biochem 283:89–98

    Article  PubMed  CAS  Google Scholar 

  • Ramalingam J, Vera Cruz CM, Kukreja K, Chittoor JM, Wu JL, Lee SW, Baraoidan M, George ML, Cohen MB, Hulbert SH, Leach JE, Leung H (2003) Candidate defense genes from rice, barley and maize and their association with qualitative and quantitative resistance in rice. Mol Plant Microbe Interact 16:14–24

    Article  PubMed  CAS  Google Scholar 

  • Ren X, Wang X, Yuan H, Weng Q, Zhu L, He1 G (2004) Mapping quantitative trait loci and expressed sequence tags related to brown planthopper resistance in rice. Plant Breed 123:342–348

    Article  CAS  Google Scholar 

  • Rojo E, Leon J, Sanchez-Serrano JJ (1999) Cross-talk between wound signaling pathways determines local versus systemic gene expression in Arabidopsis thaliana. Plant J 20:135–142

    Article  PubMed  CAS  Google Scholar 

  • Romero GO, Simmons C, Yaneshita M, Doan M, Thomas BR, Rodriguez RL (1998) Characterization of rice endo-ß-glucanase genes (Gns2-Gns14) defines a new subgroup within the gene family1. Gene 223:311–320

    Article  PubMed  CAS  Google Scholar 

  • Sardesai N, Subramanyam S, Nemacheck J, Williams C (2005) Modulation of defense response gene expression in wheat during Hessian fly larval feeding. J Plant Interact 1:39–50

    Article  CAS  Google Scholar 

  • Sogawa K (1982) The rice brown planthopper: Feeding physiology and host plant interactions. Annu Rev Entomol 27:49–73

    Article  CAS  Google Scholar 

  • Sogawa K, Liu GJ, Shen JH (2003) A review on the hyper-susceptibility of Chinese hybrid rice to insect pests. Chin J Rice Sci 17:23–30

    Google Scholar 

  • Stacey J, Isaac P (1994) Isolation of DNA from plants. In: Isaac PG (ed) Methods in molecular biology, vol. 28. Protocols for nucleic acid analysis by non-radioactive probes, Humana Press, Totowa, pp 9–15

    Google Scholar 

  • Stone SL, Hauksdottir H, Troy A, Herschleb J, Kraft E, Callis J (2005) Functional analysis of the RING-type ubiquitin ligase family of Arabidopsis. Plant Physiol 137:13–30

    Article  PubMed  CAS  Google Scholar 

  • Su CC, Zhai HQ, Cheng XN, Wan JM (2002) Detection and analysis of QTLs for resistance to brown planthopper, Nilaparvata lugens (Stål), in rice (Oryza sativa L.), using backcross inbred lines. Rice Genet Newsl 19:88–89

    Google Scholar 

  • Vitte C, Talag JD, Panaud O, Bernardo MA, Brar DS (2003) Development of O. minuta specific clones using representational difference analysis (RDA). Rice Genet Newsl 20:121–122

    Google Scholar 

  • Volkov RA, Panchuk II, Schöffl F (2003) Heat-stress-dependency and developmental modulation of gene expression: the potential of house-keeping genes as internal standards in mRNA expression profiling using real-time RT-PCR. J Exp Bot 54:2343–2349

    Article  PubMed  CAS  Google Scholar 

  • Walling LL (2000) The myriad plant responses to herbivores. J Plant Growth Regul 19:195–216

    PubMed  CAS  Google Scholar 

  • Wang X-L, He R-F, He G-C (2005) Construction of suppression subtractive hybridization libraries and identification of brown planthopper-induced genes. J Plant Physiol 162:1254–1262

    Article  PubMed  CAS  Google Scholar 

  • Watanabe T, Kitagawa H (2000) Photosynthesis and translocation of assimilates in rice plants following phloem feeding by the planthopper Nilaparvata lugens (Homoptera: Delphacidae). J Econ Entomol 93:1192–1198

    Article  PubMed  CAS  Google Scholar 

  • Xu XF, Mei HW, Luo LJ, Cheng XN, Lin ZK (2002) RFLP-facilitated investigation of the quantitative resistance of rice to brown planthopper (Nilaparvata lugens). Theor Appl Genet 104:248–253

    Article  PubMed  CAS  Google Scholar 

  • Yamagata H, Uesugi M, Saka K, Iwasaki T, Aizono Y (2000) Molecular cloning and characterization of a cDNA and a gene for subtilisin-like serine proteases from rice (Oryza sativa L.) and Arabidopsis thaliana. Biosci Biotechnol Biochem 64:1947–1957

    Article  PubMed  CAS  Google Scholar 

  • Yan J, Wang J, Zhang H (2002) An ankyrin repeat-containing protein plays a role in both disease resistance and antioxidation metabolism. Plant J 29:193–202

    Article  PubMed  CAS  Google Scholar 

  • Yang H, You A, Yang Z, Zhang F, He R, Zhu L, He G (2004) High-resolution genetic mapping at the Bph15 locus for brown planthopper resistance in rice (Oryza sativa L.). Theor Appl Genet 110:182–191

    Article  PubMed  CAS  Google Scholar 

  • Yu J, Hu S, Wang J, Wong GK, Li S, Liu B, Deng Y, Dai L, Zhou Y, Zhang X, Cao M, Liu J, Sun J, Tang J, Chen Y, Huang X, Lin W, Ye C, Tong W, Cong L, Geng J, Han Y, Li L, Li W, Hu G, Huang X, Li W, Li J, Liu Z, Li L, Liu J, Qi Q, Liu J, Li L, Li T, Wang X, Lu H, Wu T, Zhu M, Ni P, Han H, Dong W, Ren X, Feng X, Cui P, Li X, Wang H, Xu X, Zhai W, Xu Z, Zhang J, He S, Zhang J, Xu J, Zhang K, Zheng X, Dong J, Zeng W, Tao L, Ye J, Tan J, Ren X, Chen X, He J, Liu D, Tian W, Tian C, Xia H, Bao Q, Li G, Gao H, Cao T, Wang J, Zhao W, Li P, Chen W, Wang X, Zhang Y, Hu J, Wang J, Liu S, Yang J, Zhang G, Xiong Y, Li Z, Mao L, Zhou C, Zhu Z, Chen R, Hao B, Zheng W, Chen S, Guo W, Li G, Liu S, Tao M, Wang J, Zhu L, Yuan L, Yang H (2002) A draft sequence of the rice genome (Oryza sativa L. ssp. indica). Science 296:79–92

    Article  PubMed  CAS  Google Scholar 

  • Yuan H, Chen X, Zhu L, He G (2004) Isolation and characterization of a novel rice gene encoding a putative insect-inducible protein homologous to wheat Wir1. J Plant Physiol 161:79–85

    Article  PubMed  CAS  Google Scholar 

  • Yuan H, Chen X, Zhu L, He G (2005) Identification of genes responsive to brown planthopper Nilaparvata lugens Stål (Homoptera: Delphacidae) feeding in rice. Planta 221:105–112

    Article  PubMed  CAS  Google Scholar 

  • Zhang F, Zhu L, He G (2004) Differential gene expression in response to brown planthopper feeding in rice. J Plant Physiol 161:53–62

    Article  PubMed  CAS  Google Scholar 

  • Zhu-Salzman K, Salzman RA, Ahn JE, Koiwa H (2004) Transcriptional regulation of Sorghum defense determinants against a phloem-feeding aphid. Plant Physiol 134:420–431

    Article  PubMed  CAS  Google Scholar 

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Acknowledgments

This work was supported, in part, by grants from the Crop Functional Genomic Center (CG1512, CG1422), the 21 Century Frontier Program, from the Biogreen 21 Program, Rural Development Administration, and from SRC for the Plant Metabolism Research Center (PMRC), Korea Science and Engineering Foundation (KOSEF) Program.

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Correspondence to Dong-Soo Park.

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Communicated by T. Tai.

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Park, DS., Lee, SK., Lee, JH. et al. The identification of candidate rice genes that confer resistance to the brown planthopper (Nilaparvata lugens) through representational difference analysis. Theor Appl Genet 115, 537–547 (2007). https://doi.org/10.1007/s00122-007-0587-0

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